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Matsucoccus Macrocicatrices FOREST ENTOMOLOGY Matsucoccus macrocicatrices (Hemiptera: Matsucoccidae): First Report, Distribution, and Association With Symptomatic Eastern White Pine in the Southeastern United States ANGELA M. MECH,1,2 CHRISTOPHER ASARO,3 MICHELLE M. CRAM,4 DAVID R. COYLE,1 5 6 1 PENELOPE J. GULLAN, LYN G. COOK, AND KAMAL J. K. GANDHI J. Econ. Entomol. 106(6): 2391Ð2398 (2013); DOI: http://dx.doi.org/10.1603/EC13251 ABSTRACT We provide the Þrst report of Matsucoccus macrocicatrices Richards (Hemiptera: Mat- sucoccidae) feeding and reproducing on eastern white pine, Pinus strobus L., in the southeastern United States. Until now, M. macrocicatrices had been reported only from the Canadian Atlantic Maritimes, New Hampshire, and Massachusetts. Entomological holdings of 27 major museums in eastern North America have no historical records for M. macrocicatrices from the southeastern region. However, our Þeld surveys and molecular analyses (DNA barcoding) have resulted in the collection and positive identiÞcation of M. macrocicatrices in Georgia, North Carolina, South Carolina, Tennessee, Virginia, and West Virginia. In addition to the new geographic range, M. macrocicatrices is also being associated with dieback and mortality of all diameter classes of P. strobus leading to concern about a potential shift from its historically nonpestiferous presence on the host tree. On P. strobus, M. macrocicatrices was found embedded in cankers or present on top of the bark with necrotic tissue under their feeding area, indicating that they may be creating wounds for opportunistic pathogenic fungi to infest. Further, we found M. macrocicatrices living outside of the epiphytic mats of its symbiotic fungus, Septobasidium pinicola Snell. This study shows that M. macrocicatrices is now widespread in the southeastern United States, with implications for the future survival and regeneration of P. strobus in eastern North America. KEY WORDS eastern white pine, Matsucoccidae, Matsucoccus macrocicatrices, Pinus strobus, south- eastern United States The genus Matsucoccus Cockerell, commonly known recently been synonymized (Morrison 1939, Parr as the pine bast scales or matsucoccids (Hemiptera: 1939, Richards 1960, Watson et al. 1960, Ray and Wil- Coccoidea: Matsucoccidae), is a group of widely dis- liams 1991, Kosztarab 1996, Booth and Gullan 2006; tributed scale insects in temperate, tropical, and sub- Table 1). Among these scale species, M. gallicolus has tropical areas of the world. There are 32 extant Mat- the widest native host and distribution range in east- sucoccus species worldwide, with 19 in North America ern North America. M. alabamae is reported only from that all feed exclusively on trees in the Pinaceae family pine trees in Alabama; M. banksianae from jack pine (BenÐDov 2005, 2012). Eastern North American for- (Pinus banksiana Lambert) in Minnesota; M. macro- ests have Þve species of Matsucoccus: 1) Matsucoccus cicatrices from eastern white pine (Pinus strobus L.) in alabamae Morrison; 2) Matsucoccus banksianae Ray the Canadian Maritime Provinces, New Hampshire, and Williams; 3) Matsucoccus gallicolus Morrison; 4) and Massachusetts; and M. matsumurae from red pine Matsucoccus macrocicatrices Richards; and 5) Matsu- (Pinus resinosa Aiton) in Connecticut, Massachusetts, coccus matsumurae (Kuwana), a nonnative species for New Hampshire, New Jersey, New York, Pennsylva- which Matsucoccus resinosae Bean and Godwin has nia, and Rhode Island (Table 1). Several Matsucoccus species are known to be pes- 1 Daniel B. Warnell School of Forestry and Natural Resources, tiferous and economically important, as their feeding University of Georgia, 180 East Green St., Athens, GA 30602. activities have been implicated in dieback and mor- 2 Corresponding author, e-mail: [email protected]. tality of both mature and young pine trees. For ex- 3 Virginia Department of Forestry, 900 Natural Resources Drive, ample, in the southwestern United States, the pinyon Suite 800, Charlottesville, VA 22903. 4 USDA Forest Service, Forest Health Protection, 320 Green St., needle scale, Matsucoccus acalyptus Herbert, can cause Athens, GA 30602. defoliation and mortality of pinyon pine (Pinus edulis 5 Division of Evolution, Ecology and Genetics, The Research Engelmann) after repeated feeding (McCambridge School of Biology, The Australian National University, Canberra, ACT and Pierce 1964). The nonnative M. matsumurae was 0200, Australia. 6 School of Biological Sciences, The University of Queensland, responsible for foliage discoloration (Bean and God- Brisbane, QLD 4072, Australia. win 1955) and mortality of plantation-grown P. res- 2392 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 106, no. 6 Table 1. Pine hosts and collection localities of Matsucoccus scale species documented in eastern North America Collection locality in eastern North Scale species Pine hosts in eastern North America Citations America M. alabamae Pinus spp. Alabama Morrison (1939), Drooz (1985) Morrison M. banksianae P. banksiana Lambert Minnesota Ray and Williams (1991) Ray & Williams M. gallicolus P. echinata Miller, P. elliottii Connecticut, District of Columbia, Florida, Morrison (1939), Parr (1939), Morrison Engelm., P. glabra Walter, Georgia, Kentucky, Massachusetts, Drooz (1985), Kosztarab P. ponderosa Douglas ex Lawson, Maryland, Maine, Missouri, North (1996) P. pungens Lambert, P. resinosa Carolina, New Hampshire, New Jersey, Aiton, P. rigida Miller, P. serotina New York, Ohio, Pennsylvania, Rhode Michaux, P. taeda L., P. virginiana Island, Tennessee, Virginia Miller M. macrocicatrices P. strobus L. Massachusetts, New Brunswick, New Richards (1960), Watson et al. Richards Hampshire, Nova Scotia, Ontario, (1960), Martineau (1964), Quebec Drooz (1985), Kosztarab (1996), Foldi (2004) M. matsumurae P. densiflora Siebold & Zuccarinia, Connecticut, Massachusetts, New Bean and Godwin (1955, 1971), (Kuwana) P. resinosa, P. rigida, P. Hampshire, New Jersey, New York, Drooz (1985), Kosztarab tabulaeformis Carrie`rea, P. Pennsylvania, Rhode Island (1996), Li and Zhao (1997), thunbergii Parlatorea New Hampshire Division of Forests and Lands (2012), USDA Forest Service, Forest Health Protection (2013) a Asian pine species. inosa in Connecticut (McClure 1983). M. gallicolus a number of vertebrate wildlife species for food, pro- was responsible for killing terminal leaders on Ͼ63% tection, and shelter (Wendel and Smith 1990). In of pitch pine (Pinus rigida Miller) trees in Pennsyl- addition, P. strobus is commercially valuable as both a vania, and caused Ͼ50% mortality in pitch pine stands timber and Christmas tree species in the United States in Massachusetts (Parr 1939). (Wendel and Smith 1990). In the northeastern region Recently, eastern white pine (P. strobus) trees in of the United States, P. strobus is one of the most mixed and pure stands started showing dieback in the harvested conifer species and is listed as having the Appalachian Mountains of Virginia (2006) and Geor- highest volume of sawtimber in four states (Maine, gia (2011). Symptoms included branch ßagging, Massachusetts, New Hampshire, and Rhode Island; crown thinning, resinosis at branch crotches and on Butler et al. 2012a,b; McCaskill and McWilliams 2012; the main stem, and cankers on all diameter classes of Morin and Woodall 2012). trees. Follow-up visits to several locations revealed an Similar to Georgia and Virginia, dieback and mor- increase in the number of symptomatic trees as well as tality of P. strobus has also been reported in Maine, tree mortality. On close inspection of branches and New Hampshire, Ontario, and West Virginia, and has main stems, small black immature stages of a scale been attributed largely to pathogens such as Calici- insect were found embedded in the majority of the opsis pinea Peck (Lombard 2003, Maine Forest Service cankers, under lichen, and in branch crotches (Fig. 1A 2008, Rose 2011, Llewellyn 2013). Examination of and B). In 2007, scale specimens from Bath County, symptomatic P. strobus samples from New Hampshire VA, were sent to the Florida Department of Agricul- and West Virginia revealed immature insects of a Mat- ture and Consumer Services where they were tenta- tively identiÞed as an immature instar of a Matsucoccus sucoccus species embedded in the majority of the can- species based on morphological characteristics (G. kers, including the C. pinea cankers. A cursory exam- Hodges, personal communication). The taxonomy of ination of the fungi associated with cankers and Matsucoccus is based on adult females and immature feeding scales of Matsucoccus on P. strobus in Virginia cyst-stage specimens cannot be identiÞed to species revealed the presence of a number of common, op- based on morphology. The only known Matsucoccus portunistic, typically nonaggressive fungal pathogens scale to use P. strobus as a host is M. macrocicatrices, but including C. pinea, Diplodia scrobiculata de Wet, Slip- this species has never been documented as being as- pers & WingÞeld, Fusarium chlamydosporium Wol- sociated with severe dieback or mortality of the host lenw. & Reinking, and Fusarium acuminatum Ellis & tree, nor has it been reported south of Massachusetts. Everh. (Cram et al. 2009). P. strobus is a long-lived, ecologically and econom- Our research objectives were to: 1) identify the ically important conifer species in North America with Matsucoccus species present on symptomatic P. stro- a native range encompassing 31 states and provinces bus; 2) determine the geographic distribution of this (Fig. 2). It is a dominant or codominant tree
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